The epidermis of Phoronis psammophila Cori (Phoronida, Lophophorata):
an ultrastructural and histochemical study
I.. FERNANDEZ,
A. AGUIRRE,
F. PARDOS,C. ROLDAN,
J. BENITO,AND C. C. EMIG
Departamento de Biologia Animal I, Facultad de Biologia, Universidad Complutense, E-28040 Madrid, Spain
Received July 12, 1990
I., AGUIRRE,A., PARDOS,F., ROLDAN,C., BENITO,J., and EMIG,C. C. 1991. The epidermis of Phoronis
FERNANDEZ,
psammophila Cori (Phoronida, Lophophorata): an ultrastructural and histochemical study. Can. J. Zool. 69: 2414-2422.
The principal cell types of the trunk epidermis of Phoronis psammophila are categorized and described on the basis of their
ultrastructural and histochemical properties. There are seven cell types: uniciliated supporting cells with a well-developed
microvillar layer, fine-granule-containingcells with distinctive finger-like processes that contain vesicles and extend into the
microvillar layer, and five types of generalized gland cells distinguished mainly by the fine structure of their secretory
granules. Gland cells lack cilia but possess intact basal body complexes within the cytoplasm in close association with the
Golgi complex. This is an unusual feature for gland cells, and suggests that they may have recently evolved from more typical
ciliated epithelial cells. The secretory product of the gland cells contains either acidic mucopolysaccharides, which are mostly
sulfated, or neutral mucopolysaccharides and protein. The possible functions of these cell types are discussed. The supporting
cells are presumably involved in direct uptake of nutrients and (or) the protection and cleaning of the epidermis. The finegranule-containing cells may help the animal adhere to the tube, whereas the gland cells probably function in the secretion
of the tube.
FERNANDEZ,
I., AGUIRRE,A., PARDOS,F., ROLDAN,C., BENITO,J., et EMIG,C. C. 1991. The epidermis of Phoronis
psammophila Cori (Phoronida, Lophophorata): an ultrastructural and histochemical study. Can. J. Zool. 69 : 2414-2422.
L'Cpiderme du tronc de Phoronis psammophila est composC de sept types cellulaires, dCcrits d'aprks leurs caractkristiques
ultrastructurales et histochimiques : cellules de soutien monociliCes B microvillositCs bien dCveloppCes, cellules B granules fins,
B digitations dans la bordure en brosse, et cinq types de cellules glandulaires distinctes surtout par la microstructure de leurs
granules sCcrCteurs. MalgrC l'absence d'un cil externe, les cellules glandulaires posskdent des structures ciliaires basales en
Ctroite relation avec l'appareil de Golgi. Ces structures, rares dans les cellules glandulaires, permettent de croire B 1'Cvolution
rCcente de ces cellules B partir de cellules CpithCliales monociliCes typiques. Les sCcrCtions sont soit des mucopolysaccharides
acides, de type sulfate, soit des mucopolysaccharides neutres associCs B des protCines. Les fonctions possibles des diffkrents
types cellulaires sont examinCes. Les cellules de soutien interviennent probablement dans l'absorption directe des nutriments
ainsi que dans la protection et le nettoyage de 1'Cpiderme; les cellules B granules-fins semblent faciliter 1'adhCsion de l'animal
(en position normale) B son tube; les cellules glandulaires semblent principalement responsables de la formation et de
l'entretien du tube.
Introduction
Araldite via propylene oxide. The blocks were sectioned with an LKB
I11 ultramicrotome. After staining in lead citrate, the sections were
The Phoronida are tubicolous and free living within their
viewed and photographed using a Philips EM 201 electron microtubes. The tube of Phoronis psammophila Cori is composed of
scope.
sand grains and various particles aggregated by epidermal - For histochefical tests, the specimens were embedded in paraffin
secretions. The epidermis of phoronids is a simple epithelium,
wax after fixation in neutral buffered formalin or Bouin's fluid. The
the cells of which are taller in the trunk region of the body
blocks were sectioned at 5-7 p,m. The following histochemical
than in the ampulla and tentacles. The epidermal cells contain
techniques were used (for details see Lison 1960; Pearse 1968; Gabe
a brush border of microvilli (Emig 1971) and rest upon a
1968): for mucopolysaccharides:periodic acid - Schiff (PAS); Alcian
Blue 8GX (AB) at pH 2.5 and 1.5; AB-PAS; Toluidine Blue (TB) at
basement membrane. A basiepithelial nerve plexus occurs
pH 4.2-1.5. For chemical conversion the techniques of methylation
among the epidermal cells. Several types of epidermal cells,
and sequential methylation-saponification (KOH) were used. The
including gland cells which are mainly involved in tube
enzyme
was hyaluronidase (from ovine testes; Sigma); for proteins:
secretion, have been previously identified, using light microsthe tetrazo reaction, with or without previous treatment by dinitrocopy, in the body wall of the same species (see Pourreau 1979;
fluorobenzene (DNFB), performic oxidation, benzoylation, and
Emig 1982).
deamination.
This paper is the first ultrastructural investigation of a
phoronid epidermis to provide a detailed description of the
Results
various cell types and their distribution along the body wall.
The epidermis of Phoronis psammophila consists of several
The ultrastructure and histochemistry are discussed with
cell types: supporting cells, fine-granule-containing (FG) cells,
reference to previous observations on the behavior and natural
and at least five types of gland cells (Figs. 1, 2). The epiderhistory of phoronids.
mal cells are joined to one another by zonulae adhaerentes near
the apical suaace and by septate junctions below. InterdigitaMaterial and methods
tions of the lateral cell membranes also occur.
Adult Phoronis psammophila were collected along the Spanish
Numerous basiepithelial nerve cell processes containing both
Atlantic coast, in the intertidal zone of the Meira beach, Ria de Vigo,
clear
and dense-core vesicles lie directly above the basement
in northeastern Spain.
membrane. The sing1e giant nerve fiber lies in the epidermis
The specimens were fixed in 4% glutaraldehyde buffered with
on the left side of the trunk in P- psammophila (Fig. 3A)- The
0.1 M cacodylate (pH 7.4) and postfixed in 1% osmium tetroxide in
fiber is surrounded by a myelin-like sheath consisting of
seawater. Pieces of tissue were then dehydrated in acetone, stained en
bloc with 2% uranyl acetate during dehydration, and embedded in
spirally arranged and irregularly spaced lamellae (Fig. 38).
Printed in Canada 1 Imprim6 au Canada
FERNANDEZ ET AL.
Neighboring cells, possibly glial cells, appear to form an
additional sheath. In transverse section the lamellae exhibit a
pattern of major and minor bands like that of vertebrate
myelin.
Supporting cells
The term supporting cell is used here for epidermal cells that
are specialized as neither gland cells nor FG cells.
The supporting cells have a well-developed brush border of
regularly spaced microvilli covered by a moderately electrondense mucoid glycocalyx. The glycocalyx is composed of
filaments oriented parallel to the epidermal surface, where they
pass among the microvilli, and perpendicular to it over the
brush border (Figs. 1, 2, 4). Long bundles of filaments inside
the microvilli extend deep within the cell. Numerous pinocytotic invaginations are present among the bases of the microvilli
and appear to be forming coated vesicles. Pinocytotic vesicles
also occur at some distance from the apical plasma membrane
in close association with multivesicular bodies.
Supporting cells bear a single centrally located cilium (Figs.
4, 5), with the usual 9 X 2 + 2 pattern of microtubules, a
diplosomal basal body (i.e., with both a proximal and a distal
centriole), and two striated rootlets. The largest rootlet is
directed basally and the secondary rootlet extends parallel to
the cell surface. Apical to the nucleus (Figs. 1, 2), spherical
membrane-bound granules (about 0.5 p,m) with homogeneous
electron-dense material occur in gssociation with the Golgi
apparatus, which in turn lies near the basal complex of the
cilium. Other organelles, e.g., free ribosomes, rough endoplasmic reticulum (RER), and mitochondria with a dense matrix,
are also present (Figs. 4, 5). Cells extruding large amounts of
cytoplasmic material and granules have been observed, but
these may be abnormal or dying cells (Fig. 6).
Large bundles of longitudinally oriented' filaments occur in
the basal region of the supporting cells. They are attached by
hemidesmosome-like junctions to the basal cell membrane,
which in turn lies directly above the relatively thick collagenous basal lamina (Fig. 7).
Fine-granule-containing cells
The elongated FG cells increase in number from the anterior
(upper) trunk region down to the ampulla where they are
abundant (Figs. 1, 2, 8). Each cell bears a single cilium with
a diplosomal basal body and a striated rootlet (Fig. 9). The
cytoplasm is nearly filled with small ovoid granules (0.3 X
0.1 p,m on average) that contain electron-dense material. The
FG cells are expanded apically, with a variable number of
lobular, finger-like processes that extend beyond the epidermal
surface but below the tips of the microvilli (Figs. 8, 9, 14).
These apical extensions -are filled with the same ovoid electron-dense granules as the rest of the cell and each is encircled
by a collar of microvilli belonging to the neighboring supporting cells (Figs. 10, 14). Other cell organelles, i.e., free ribosomes, RER, mitochondria, and an apical Golgi complex, are
also present. The nucleus, which is ovoid and elongated, is
located in the basal third of the cell and contains abundant
heterochromatin.
Gland cells
land cells are interspersed among the supporting cells.
Each cell has an apical concavity lined by very short microvilli. The nucleus and most of the cytoplasmic organelles are
located in the basal region of the cell. Ciliary basal structures
association with the Golgi complex are present, although a
ciliary axoneme is lacking.
2415
On the basis of the histochemical data, the gland cells are
divided into two main classes: acidic mucus (AM) cells and
non-acidic mucus (NAM) cells. Based mainly on the fine
structure of their secretory granules, a total of five cell types
can be identified: AM1, AM2, NAM1, NAM2, and NAM3
cells (Table 1).
Acidic mucus cells
AM cells secrete acidic mucopolysaccharides. This is shown
by their strong metachromatic response with TB at pH 4.5 and
an intense alcianophilia with AB at pH 2.5. The resistance of
the metachromasia to dehydration and its retention below pH
3 indicate that the acidic mucopolysaccharide is sulfated. This
hypothesis is supported by an observed alcianophilia at pH 1.5,
by the susceptibility of the TB metachromasia to methylation,
and by the fact that a weak metachromasia is restored upon
subsequent saponification. The weakness of this reaction
suggests the presence of carboxyl groups.
Secretory granules were PAS negative and sometimes
weakly stained, and the response to the combined AB-PAS
technique indicated that the acidic mucosubstance predominates, i.e., the granules are strongly alcianophilic. However, a
blue-purple color, suggesting the presence of a neutral
mucosubstance, appeared occasionally.
Hyaluronidase, applied for 4-26 h at 37°C prior to AB
treatment, did not abolish the response to AB, so the positive
histochemical results to testing for acidic mucosubstances are
not due to the presence of hyaluronic acid.
All tests for protein were negative.
The AM1 cell type: AM1 cells constitute the most abundant
gland cell type in the anterior trunk epidermis (Table 1). They
are filled with low to moderately electron-dense, membranebounded secretory granules (0.6-1 p,m in diameter) (Fig. 11).
The contents have a finely fibrillar substructure with randomly
arranged darker strands, giving the granules a mottled appearance (Fig. 12). Maturing cells have an RER system containing
moderately electron-dense material and a prominent, cupshaped Golgi complex. Numerous small vesicles and condensing vacuqles enclosing fibrillar material occur near the mature
face and lateral edges of the Golgi cisternae (Figs. 11, 12).
The AM2 cell type: AM2 cells, scattered mainly in the
median and posterior trunk regions (Table I), contain rounded
to polygonal secretory granules (ca. 0.8 p,m in diameter) of
moderate electron density and homogeneous appearance. Some
granules, however, exhibit a mottled substructure. The welldeveloped Golgi complex is apical and lateral in position (Figs.
1, 2, 13, 15, 17, 21). Micrographs showing the extrusion of the
secretory product suggest an apocrine mechanism (Fig. 16).
Non-acidic mucus cells
The results of tests for acidic mucopolisaccharides were all
negative in NAM cells, but the presence of neutral mucopolysaccharides is indicated by the positive reaction obtained with
the PAS test. The number of positive cells and the degree of
response were not uniform. Positive results for proteins were
obtained using the tetrazo reaction, and the presence of tyrosine and tryptophan was detected by previous chemical conversion with DNFB and performic acid. The absence of histidine is supported by the negative results of the benzoylationtetrazo reaction.
The NAMl cell type: NAMl cells (Fig. 1) are more numerous in the middle and posterior regions of the trunk (Table 1).
They are completely filled with secretory granules (about 1.52 p,m in diameter), which are spherical, or polyhedric as a
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CAN. 1. ZOOL. VOL. 69, 1991
TABLE1. Distribution of the gland cells and fine-granule-containing
cells along the trunk epidermis of Phoronis psammophila
Cells
AM1
AM2
NAM1
NAM2
NAM3
FG
Anterior
Middle
Posterior
++++ +++ ++
0
++
0
0
+++ +++ +++
++ +++ +++ ++ ++
+
++ ++ ++
0
++ +++ +++ +++
+
++ ++ ++
+
+
Ampulla*
++
0
+++
++
+++
+++
*Excludes the posterior part o f the ampulla where mostly supporting cells occur.
result of compression. The granules have either a single large
dark core or several smaller ones distributed throughout a
homogeneous paler matrix (Fig. 17). Both the matrix and the
cores show a paracrystalline substructure (Fig. 18). NAMl
cells contain numerous free ribosomes, mitochondria, a welldeveloped RER with swollen cisternae, but a poorly developed
Golgi complex. Extrusion of the secretory product appears to
be apocrine.
The NAM2 cell type: NAM2 cells (Fig. 1) increase in
number toward the posterior trunk region (Table 1). They
contain generally ellipsoidal secretory granules (2 X 1 p,m)
whose contents have a distinct, banded substructure (Fig. 19,
20). Immature granules contain filamentous bundles of
moderate electron density (Fig. 20). NAM2 cells contain
numerous free ribosomes and highly dilated RER cisternae
enclosing a moderately electron-dense material. The Golgi
saccules appear to be closely associated with the RER.
The NAM3 cell type: NAM3 cells are numerous from the
middle trunk region to the ampulla (Table 1). The secretory
granules are characterized by a homogeneous and highly
electron-dense material. They become larger toward the apex
of the cell and subsequently coalesce to form a large secretory
mass within the cell (Figs. 1, 2, 21). The extrusion process
apparently proceeds by an apocrine mechanism (Fig. 22).
Following the extrusion NAM3 cells sometimes exhibit a dense
cytoplasm, which may indicate cellular morbidity.
Discussion
The epidermis of Phoronis psammophila contains a variety
of specialized cell types. Only the supporting cells and fine-
granule-containing cells bear cilia, although in all gland cells,
intact ciliary basal complexes occur, usually associated with
the Golgi apparatus. These basal complexes could be remnants
of the primitive ciliated epithelial cells from which the gland
cells are supposed to have evolved. The hypothesis that the
gland cells originate from supporting ciliated cells has been
suggested for other marine invertebrates (e.g., enteropneusts,
see Atarnanova 1978; Pardos and Benito 1989). Throughout the
epidermis, the cilia have the classical 9 X 2 + 2 pattern of
microtubules. They probably have at least two important
functions: (i) cleaning the surface of the epidermis and the
space between it and the tube, using a ciliary-mucoid mechanism of removing waste (e.g., the material extruded by the
supporting cells); and (ii) producing a continuous water flow
within the tube (Emig 1982) for gas and nutrient exchange,
which would also help in waste removal.
The well-developed brush border of microvilli with the
associated glycocalyx coat may have several functions,
including increasing the epithelial surface for direct uptake of
dissolved organic substances through the epidermis (Emig and
Thouveny 1976), and functioning in respiratory gas exchange,
as has recently been found for the lophophoral brush border in
the same species (Pardos et al. 1991). The bundles of filaments
inside the microvilli undoubtedly function as a cytoskeleton to
maintain the structural integrity of the brush border.
The glycocalyx .is generally covered by a mucoid coat
histochemically resembling the secretory content of AM cells.
The secretory product of these cells is an acidic mucopolysaccharide which is predominantly sulfated, with a few carboxylated groups and neutral mucopolysaccharides. Ultrastructurally ,
cells containing granules that are intermediate between those
found in AM1 and AM2 cells have sometimes been observed.
This suggests that these two cell types may be different
developmental stages of a single gland cell type. This is further
supported by the variable response of their secretion to
histochemical tests. We suggest that the AM cells may be
involved in lubricating the trunk and thus minimizing abrasion
when the animal is moving in its tube. The absence of protein
-and hyaluronic acid suggests that the secretory product has a
low viscosity, which could facilitate the formation of a film for
gaseous exchange. AM cells correspond to the B-cell type
described by Pourreau (1979). Histological tests have suggested
that these cells secrete the thick central coating layer of the
tube (Pourreau 1979; Emig 1982).
ABBREVIATIONS:
AM1 and AM2, acidic mucopolysaccharide cell types 1 and 2, respectively; Bc, basal complex; bm, basement membrane;
c, cilium; co, dense core in secretory granules; F, fingerlike extensions of the fine-granule-containing(FG) cells; G, Golgi complex; GF, giant
nerve fiber; G1, glycocalix; Ms, myelin sheath; Mv, microvilli; N, nerve fibers; NAM1, NAM2, and NAM3, non-acidic mucopolysaccharide
cell types 1, 2, and 3, respectively; R, rough endoplasmic reticulum; SC, supporting cell; SG, secretory granule.
FIG. 1. Diagram of the epidermis of Phoronis psammophila.
FIG.2. General view of a longitudinal section of the epidermis of Phoronis psammophila, showing several AM2, NAM3, and FG cells, and
one NAMl cell, among the supporting cells. Scale bar = 3 pm. FIG.3A. Cross section of the giant nerve fiber. Scale bar = 2 pm. FIG.3B.
Detail of the myelin sheath, showing its irregular packing. Scale bar = 0.1 pm. FIG.4. Apical region of a supporting cell; note the single cilium,
the brush border of microvilli, and the associated glycocalyx. Scale bar = 1 Fm. FIG.5. Golgi complex associated with the ciliary basal
structures in a supporting cell. Scale bar = 1 pm.
FIG.6. Extrusion of cytoplasmic material and granules from a supporting cell (arrow). Scale bar = 1 pm. FIG.7. Bundles of longitudinal
filaments in the basal region of a supporting cell, showing their hemidesmosome-like structures with the basement membrane (arrow). Scale
bar = 1 pm. FIG.8. Elongated FG cell filled with small ovoid electron-dense granules. Scale bar = 2 Fm. FIG.9. Apical part of an FG cell,
showing the single cilium and finger-like extensions filled with granules. Scale bar = 1 pm. FIG. 10. Cross section at the level of the brush
border, showing the arrangement of the finger-like extensions of an FG cell encircled by the microvilli of the neighboring supporting cells (see
Fig. 14). Scale bar = 1 Fm. FIG. 11. AM1 cell filled with secretory granules of varying shape and electron density. Scale bar = 2 pm. FIG.
12. Detail from Fig. 11, showing the fine fibrillar substructure with darker strands in the secretory granules and the highly developed Golgi
complex. Scale bar = 1 Fm. FIG. 13. An AM1 cell. Scale bar = 1 pm.
FERNANDEZ ET AL.
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CAN. J. ZOOL. VOL. 69, 1991
FERNANDEZ ET AL.
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CAN. J. ZOOL. VOL. 69, 1991
FIG.14. Diagram of an FG cell.
FIG.15. Secretory granules in an AM2 cell; note their mottled structure. Scale bar = 0.5 Fm. FIG.16. Extrusion of the secretory products
of an AM2 cell (arrow). Scale bar = 1 Fm. FIG. 17. An NAMl cell; the polyhedric secretory granules have single or multiple dark cores. Scale
bar = 2 Fm. FIG.18. Detail of two secretory granules of an NAMl cell, showing the paracrystalline patterns in the matrix and dense cores.
Scale bar = 0.5 Fm. FIG.19. Ellipsoidal secretory granule of an NAM2 cell with a banded substructure. Scale bar = 0.5 Fm. FIG.20. Secretory
granule production by an NAM2 cell. Note the presence of very dilated RER cisternae and secretory granules showing patches of high and low
electron density as well as banding. The arrow points to filamentous bundles in an immature granule. Scale bar = 1 Fm. FIG.21. An NAM3
cell filled with homogeneous and highly electron-dense granules. In some cases these contain flocculent fibrillar material (arrow). Scale bar =
2 Fm. FIG.22. Extrusion of secretory material by means of an apocrine mechanism in an NAM3 cell. Scale bar = 0.5 Fm.
FERNANDEZ ET AL.
242 1
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CAN. J. ZOOL. VOL. 69, 1991
NAM cell types have the cytological feature that characterizes glycoprotein-secreting cells: an extensive RER which is
associated with the Golgi complex. The histochemical tests
used in this study demonstrate the coexistence of neutral
mucopolysaccharides and proteins containing tyrosine and
tryptophan in all the NAM cell types. NAMl and NAM2 cells
show similar characteristics to the A and B' cell types described by Pourreau (1979), and their distribution is similar to
Pourreau's curve A. The NAM3 type corresponds to Pourreau's C-cells and the so-called corps-en-massue of SelysLongchamps (1907), but these cells occur all along the trunk
rather than being restricted to the base of the lophophore, as
stated by both authors. Based on the structure of the tube
(Pourreau 1979; Emig 1982), the NAM cell types are probably
involved in forming the internal and external tube layer, which
aggregates grains of sand and various types of detritus around
the tube.
In ultrastructural features, the FG cells closely resemble the
"viscid gland cells" of the duo-gland adhesive systems of
turbellarians, gastrotrichs, and some archiannelids (Boaden
1968; Tyler 1976; Martin 1978; Reuter 1978), in that the
microvilli of the neighboring supporting cells surround the
finger-like projections of the FG cells in a collar-like fashion.
Consequently, we suggest that the secretory material of the FG
cells may help the animal adhere to its tube and thus minimize
the muscular action needed to keep the phoronid extended in
the tube.
A further remarkable feature of the integumentary epithelium
is the well-developed subepidermal nerve plexus. It is most
likely that the nerve fibers control the ciliary and perhaps the
secretory activities of the epidermis. However, no sensory cells
have been recorded in the trunk epidermis, probably because
the trunk is isolated from the environment by the tube. Thus,
'stimuli are received through the sensory cells in the epidermis
of the tentacles, which are in direct contact with the surrounding medium (Pardos et al. 1991).
The giant nerve fiber in Phoronis psammophila generates a
powerful contraction of the longitudinal trunk musculature for
a quick retraction of the animal into the tube (Silkn 1954):
Further studies are obviously needed to established the detailed
construction and relationships of this giant nerve fiber.
Acknowledgement
This work was supported by the Comisi6n Interministerial
para la Ciencia y tecnologia (Research Grant No. PB 86-00 10).
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